- Email: [email protected]
The relationship of phantom limb pain to other phantom limb phenomena in upper extremity amputees1
Pain 72 (1997) 87–93
The relationship of phantom limb pain to other phantom limb phenomena in upper extremity amputees1 Pedro Montoya a ,*, Wolfgang Larbig a, Norbert Grulke a, Herta Flor b, Edward Taub c, Niels Birbaumer a , d a
Institute of Medical Psychology and Behavioral Neurobiology, University of Tu¨bingen, Gartenstrasse 29, D-72074 Tu¨bingen, Germany b Department of Psychology, Humboldt University, Berlin, Germany c Department of Psychology, University of Alabama at Birmingham, Birmingham, USA d Department of General Psychology, University of Padova, Padova, Italy Received 1 February 1997; revised version received 24 February 1997; accepted 19 March 1997
Abstract In thirty-two unilateral upper extremity amputees with and without phantom limb pain, various phantom limb phenomena were investigated. In general, the incidence of non-painful phantom limb sensations was higher in patients with phantom limb pain than in pain-free amputees. Kinesthetic and kinetic phantom limb sensations were reported more frequently than exteroceptive cutaneous sensations. There was a significant positive correlation between phantom limb pain and stump pain. Patients more frequently assigned sensory than affective pain qualities to their phantom limb pain, whereas no differences between pain qualities were observed for stump pain. No support was found for a relationship between the presence of telescoping (i.e., shrinkage of the phantom limb) and phantom limb pain. These findings point to central as well as to peripheral factors contributing to phantom limb pain. 1997 International Association for the Study of Pain. Published by Elsevier Science B.V. Keywords: Upper extremity amputation; Phantom limb pain; Phantom limb sensation; Stump pain; Telescoping; Pain qualities
1. Introduction For many individuals, the most distressing problem after amputation is the continuing experience of phantom limb sensations, especially if these sensations are painful. According to several surveys (Carlen et al., 1978; Sherman and Sherman, 1983; Sherman et al., 1984; Jensen et al., 1985), phantom limb sensations are reported by 70–100% of amputees, and phantom limb pain occurs in 60–85% of these cases. Phantom limb sensations are commonly described as tingling, numbness, pins and needles, burning, cramping, squeezing, or itching. Changes in the length, size, temperature, volume, or position of the phantom limb are also frequently reported. About one-third of the amputee
* Corresponding author. Tel.: +49 7071 29 74226; fax: +49 7071 29 5956; email: [email protected] 1 This work was supported by the Deutsche Forschungsgemeinschaft (Research Group ‘Clinical Psychophysiology of Pain’, Bi 195/24).
population experiences a bizarre phenomenon called telescoping (Weiss and Fishman, 1963; Katz, 1992; Jensen and Rasmussen, 1994). This process refers to the gradual shrinking of the phantom limb so that distal parts of the phantom limb seem to approach the stump; later the phantom foot or hand may seem to retract or even disappear completely into the stump, but can still be perceived as a foot or hand (Gue´niot, 1861; Henderson and Smyth, 1948). It has been postulated that the experience of telescoping is inversely related to phantom limb pain, such that telescoping is reduced or absent when phantom limb pain is present (Riddoch, 1941; Henderson and Smyth, 1948; Weiss and Fishman, 1963; Katz and Melzack, 1987; Katz, 1992; Jensen and Rasmussen, 1994). Katz and Melzack (1987) reported a single case with severe phantom limb pain who experienced telescoping of the phantom limb during electrical stimulation of both ears which was paralleled by satisfactory pain relief. The goal of the present study was to investigate some of the characteristics of painful and non-painful phantom limb
0304-3959/97/$17.00 1997 International Association for the Study of Pain. Published by Elsevier Science B.V. PII S0304-3959 (97 )0 0004-3
88
P. Montoya et al. / Pain 72 (1997) 87–93
sensations, as well as the relationship of phantom limb pain with stump pain. We sought to evaluate the question of whether phantom limb pain and phantom limb sensations are closely related.
2. Methods 2.1. Subjects Sixty-five amputees who were registered as clients of an orthopedic appliance shop that fitted amputees with prostheses were contacted by telephone. A brief interview was used to select those subjects who met the following criteria: (a) unilateral upper-limb amputation, (b) between 18 and 60 years of age, (c) absence of any diagnosed psychiatric disorder, and (d) taking no current medication. Thirty-two unilateral upper-limb amputees (three female) with a mean age of 41.0 years (SD = 11.7, range: 20–58 years) participated in the study. With the exception of two cases of congenital limb deficiency, subjects had undergone amputation as a result of an accident. The time elapsed since the traumatic amputation ranged from 10 months to 49 years, with a mean of 12.2 years (SD = 10.5). The subjects were reimbursed for travel expenses and informed consent was obtained after the nature and purpose of the study were explained. 2.2. Measures 2.2.1. Assessment of phantom limb and stump phenomena Two instruments were used to assess painful and nonpainful sensations experienced by amputees. 2.2.1.1. Phantom-and-Stump Phenomena Interview. The standardized Phantom-and-Stump Phenomena Interview developed by the authors (Flor et al., 1995) consists of 122 items that assess the location, quality, intensity, duration and frequency of phantom- and stump-related phenomena at the time of the interview and soon after amputation. It includes separate sections for painful and non-painful phantom limb sensations and for painful and non-painful stump sensations; thus, stump and phantom limb sensations were assessed separately. Phantom limb and stump pain are examined by: (a) pain descriptors based on the McGill Pain Questionnaire (Melzack, 1975) and derived from the Pain Sensitivity Scale2 (Geissner, 1997) which are scored for both appropriateness (4-point 2
This scale is a multidimensional instrument to assess the sensory and affective dimensions of pain. It consists of 24 pain descriptors which were modified from the McGill Pain Questionnaire. Both subscales show satisfactory internal consistency (Cronbachs’ a for the sensory and affective dimensions, 0.81 and 0.92, respectively) and good stability (test-retest correlations over 4 weeks, 0.95 and 0.96, respectively). For the present study, three additional descriptors (convulsive, tingling, wrenching) were included.
scale: 0 = ‘does not apply’, 1 = ‘applies a little’, 2 = ‘quite appropriate’, 3 = ‘applies exactly’), and frequency of occurrence (9-point scale: 0 = ‘never’ to 8 = ‘always’); (b) a 10-cm visual analogue scale (VAS) that describes the average intensity of pain ranging from ‘no pain’ to ‘unbearable pain’; and (c) a stylized human figure drawing on which the locations of regions of stump and phantom limb in which pain is experienced are indicated. In addition, non-painful stump and phantom limb sensations are assessed in the interview using: (a) 13 descriptors of sensations including kinesthetic (e.g., ‘I feel the size of the phantom limb’), kinetic (e.g., ‘I feel voluntary movements of the phantom limb’), and exteroceptive (e.g., ‘I feel pressure on the phantom limb’) sensations; each des-criptor was scored for both intensity (4-point scale: 0 = ‘no sensation’ to 3 = ‘very strong sensation’) and fre-quency (9-point scale: 0 = ‘never’ to 8 = ‘always’); (b) a 10-cm VAS to describe the average intensity of non-painful phantom limb and stump sensations ranging from ‘no sensation’ to ‘very strong sensation’; (c) a stylized human figure drawing to record the body regions from which non-painful phantom limb sensations were elicited and the location of regions of stump and phantom limb in which non-painful phantom or stump sensations were experienced; and (d) open-ended questions about possible factors influencing phantom limb and stump sensations. Additional items elicited detailed information about the presence of telescoping, the amount of telescoping (measured by calculating the distance from the phantom fingertips to the stump and referred to the intact arm), and the intensity and frequency of telescoping. 2.2.1.2. The West Haven-Yale Multidimensional Pain Inventory. The scales Pain Severity, Interference, and Support of The West Haven-Yale Multidimensional Pain Inventory (MPI; Kerns et al., 1985; German version Flor et al., 1990) were completed separately for stump and phantom limb pain experienced during the last week. 2.2.2. Evaluation of mental imagery. Patients’ ability to imagine stimuli in a variety of sensory modalities was assessed using a modified and shortened version of Betts’ Questionnaire upon Mental Imagery (QMI; Sheehan, 1967). This instrument was employed to determine whether there is a relationship between the vividness of patients’ imagery ability and the likelihood that they might experience phantom limb sensations. The original instrument investigates imagery in seven sensory modalities: visual, auditory, cutaneous, kinetic, gustatory, olfactory and organic. Subjects are instructed to consider carefully the image elicited by each item and rate its vividness on a 7-point scale (0 = ‘no image present at all’ to 6 = ‘perfectly clear and vivid’). In the present study, only items from the cutaneous (e.g., the prick of a pin) and the kinetic modalities (e.g., running upstairs) were used. In
P. Montoya et al. / Pain 72 (1997) 87–93
addition, 12 items were included to assess patients’ ability to imagine the characteristics and sensations of other persons (e.g., body form, the way of walking) and their own phantom and intact limbs (e.g., limb form, movement of the limb).
3. Results 3.1. Phantom limb pain According to the Phantom-and-Stump Phenomena Interview, 16 patients suffered from phantom limb pain both in the past and during the interview, 15 had never experienced phantom limb pain and one patient had occasionally experienced phantom limb pain during a period of 2 weeks before he left the hospital 4 months after amputation. Fourteen patients with phantom limb pain reported experiencing it since the first week after amputation. An additional patient had experienced pain for the first time more than 30 years after the amputation had been carried out. One phantom limb pain patient was not able to remember the onset of his pain. Fifteen patients reported that their phantom limb pain lasted a few seconds to minutes at a time; only one patient suffered from longer periods of pain (several hours). Phantom limb pain was experienced every day at frequent intervals by five patients (31%), while eleven (69%) reported phantom limb pain from several times per day to approximately once per week. Table 1 presents demographic characteristics of the phantom limb pain and the pain-free group. There were no significant group differences in age, time since amputation, gender, site of the amputation (above versus below elbow), or educational level. Table 1 Demographic variables
Age (years) Mean SD Range Time since amputation (years) Mean SD Range Gender Female Male Amputation site Above elbow Below elbow Educational level (school) More than 8 years Less than 8 years
Amputees with phantom limb pain (n = 16)
Amputees without phantom limb pain (n = 16)
42.3 12.5 20–58
40.0 11.2 23–57
10.6 11.3 1–49
12.2 10.2 0–36
– 16
3 13
5 11
3 13
15 1
15 1
89
3.2. Non-painful phantom limb sensations Non-painful phantom limb sensations were reported at the time of the investigation by all 16 patients with phantom limb pain and 10 patients without phantom limb pain. The difference between groups was significant (Yates corrected x2 = 7.15, P , 0.01). A significant group difference was also found in retrospective reports of non-painful phantom limb sensations shortly after the amputation; 16 phantom limb pain and 8 pain-free subjects, respectively, indicated non-painful phantom limb sensations at that time (Yates corrected x2 = 10.33, P , 0.01). Six patients (including the two congenital amputees) reported never having either painful or non-painful phantom limb sensations. In order to investigate in more detail the nature of phantom limb sensations as well as changes from the time of the amputation to the time of the interview, we computed the product (ranging from 0 to 24) of the intensity and frequency for the three categories of phantom limb sensations (kinesthetic, kinetic, exteroceptive) from the Phantom-andStump Phenomena Interview. A three-way ANOVA was performed on this measure; the between-subjects factor was Group (phantom limb pain versus no phantom limb pain) and within-subjects factors were Category (kinesthetic, kinetic, exteroceptive) and Time (shortly after amputation versus at present). A significant Category effect was found (F(2,42) = 12.7, P , 0.001, Greenhouse-Geisser epsilon = 0.9): the mean kinesthetic phantom sensation was 8.5 on a scale ranging from 0 to 24 (SD = 6.7), the mean kinetic phantom sensation was 6.7 (SD = 5.5) and the mean exteroceptive phantom sensation was 1.9 (SD = 3.0). Post-hoc analyses indicated that the magnitude of exteroceptive phantom limb sensations was significantly lower than that of kinesthetic (t-test (25) = 5.1, P , 0.001) and kinetic (t-test (25) = 5.1, P , 0.001) sensations, but there was no difference between kinesthetic and kinetic sensations (t-test (25) = 1.5, NS). A marginally significant Group effect was found (F(1,21) = 3.9, P = 0.063) for the intensity of non-painful phantom sensations: amputees with phantom limb pain tended to report more intense non-painful phantom sensations (mean = 7.3, SD = 3.8) than painfree amputees (mean = 3.1, SD = 2.9). The reason for the marginal nature of this group effect was that there was a significant difference in the intensity of non-painful phantom limb sensations between patients with phantom limb pain and those without phantom limb pain at the time of the interview (F(l,23) = 7.4, P , 0.05); but this difference between groups was not significant immediately after amputation (F(1,22) = 2.8, P . 0.1). Moreover, a significant positive correlation was found between the intensity of phantom limb pain and the magnitude (product of intensity and frequency) of non-painful phantom limb sensations (Spearman r = 0.57, P , 0.05). This provides further evidence that increased phantom limb pain is associated with stronger non-painful phantom limb sensations. A significant Time effect (F(1,21) = 4.8, P , 0.05) was present when the
90
P. Montoya et al. / Pain 72 (1997) 87–93
frequency, but not the intensity of non-painful phantom limb sensations was examined separately: non-painful phantom limb sensations were more frequent immediately after amputation (mean = 3.8 on a scale ranging from 0 to 8, SD = 1.4) than at the time of the study (mean = 3.1, SD = 1.5); this was not the case for the intensity of nonpainful phantom limb sensations. Twelve patients (of 16) with phantom limb pain and five (of 10) pain-free amputees reported telescoping of the phantom limb (Yates corrected x2-square = 1.63, NS). When it occurred, the sensation of telescoping was quite intense, and there was no difference in experienced intensity for patients with phantom limb pain (mean = 8.6 cm on a 10-cm VAS, SD = 2.2) and pain-free amputees (mean = 7.9 cm, SD = 3.7). There was also no significant group difference with respect to the length of the telescoped phantom limb measured as the percentage of shrinkage from the phantom fingertips to the stump compared to the intact arm (a value of 100% indicates that the phantom limb is perceived within Table 2 Percentage of amputees who considered the different items of the Pain Sensitivity Scale (Geissner, 1997) to be ‘quite appropriate’ or ‘applies exactly’ to describe their phantom limb pain and stump pain Phantom limb pain recalled
Sensory dimension Stabbing Beating Searing Convulsive Throbbing Hot Burning Pounding Penetrating Tingling Wrenching Cutting Tearing Affective dimension Intense Gruelling Heavy Annoying Terrible Unbearable Dreadful Cruel Torturing Wretched Exhausting Horrible Petrified Killing
Stump pain recalled
After amputation
At the time of After the interview amputation
At the time of the interview
73.3 60.0 73.3 73.3 73.3 66.7 60.0 53.3 53.3 46.7 53.3 46.7 26.7
75.0 68.8 62.5 62.5 56.3 56.3 56.3 43.8 37.5 31.3 25.0 25.0 12.5
57.1 71.4 71.4 42.9 64.3 64.3 57.1 50.0 28.6 64.3 50.0 35.7 42.9
36.4 36.4 36.4 36.4 45.5 54.5 36.4 27.3 18.2 27.3 36.4 36.4 36.4
80.0 66.7 46.7 53.3 46.7 46.7 33.3 40.0 6.7 33.3 26.7 13.3 13.3 13.3
50.0 37.5 37.5 31.3 18.8 18.8 18.8 12.5 12.5 6.3 6.3 6.3 – –
71.4 57.1 50.0 57.1 64.3 28.6 64.3 35.7 42.9 35.7 35.7 42.9 7.1 14 3
45.5 27.3 18.2 – 36.4 5.9 45.5 18.2 18.2 18.2 18.2 27.3 11.8 –
the stump; a value of 0% refers to a non-telescoped limb and indicates that the phantom limb is perceived as having the same length as the intact arm). For patients with phantom limb pain who had telescoping, the mean shrinkage was 84.2% (SD = 21.1); for pain-free amputees who had telescoping, the mean shrinkage was 99.0% (SD = 2.2) (Yates corrected x2 = 1.23, NS). 3.3. Pain Quality Table 2 presents the percentage of patients who considered each of the different adjectives of the Pain Sensitivity Scale to be ‘quite appropriate’ (score of 2 on a 0–3 numerical scale) or "apply exactly’ (score of 3) to describe their phantom limb pain (left side of table) and stump pain (right side). As can be seen, more descriptors from the sensory subscale than from the affective subscale were chosen by at least 50% of the amputees as being appropriate. In addition, adjectives used to describe pain shortly after amputation were more varied than those used to describe current pain. The mean score of the appropriateness of pain descriptors was calculated for the sensory and the affective dimensions and a two-way ANOVA3 for repeated measures was carried out separately for phantom limb pain and stump pain on this measure, the factors being Pain Quality (sensory versus affective) and Time (at present versus soon after amputation). A significant Pain Quality effect was found (F(1,13) = 25.52, P , 0.001): sensory qualities were considered more appropriate to describe phantom limb pain (mean = 1.5 on a scale ranging from 0 to 3, SD = 0.6) than affective qualities (mean = 0.9, SD = 0.6). A significant Time effect was also found (F(1,13) = 6.96, P , 0.05), indicating that all pain descriptors were considered less appropriate at the time of the interview (mean = 1.0, SD = 0.4) than they were for the recall of the pain experience at the time of the amputation (mean = 1.4, SD = 0.6). The Pain Quality × Time effect did not achieve significance (F(1,13) = 3.2, P , 0.1). No significant differences were found in the appropriateness of sensory and affective descriptors for stump pain (Pain Quality effect: F(1,10) = 2.0, NS). Moreover, both sensory and affective aspects of stump pain were considered less appropriate at the time of the interview (mean sensory = 1.2, SD = 0.6; mean affective = 0.8, SD = 0.6) as compared to the period immediately after the amputation (mean sensory = 1.7, SD = 0.7; mean affective = 1.3, SD = 0.8) (Time effect: F(1,10) = 10.7, P , 0.01). To evaluate whether patients who experienced both phantom limb and stump pain used the same or different descriptors for the two types of pain, the number of terms that were used for each type of pain was computed for each patient 3 Only patients reporting pain at both time points were included in this ANOVA, resulting in 14 patients for the analysis of phantom limb pain and 11 for stump pain.
91
P. Montoya et al. / Pain 72 (1997) 87–93 Table 3
Description of pain in patients experiencing both phantom limb and stump pain. Number of adjectives used to describe pain from the Pain Sensitivity Scale (Geissner, 1997) that were considered by the patients as ‘quite appropriate’ or ‘applies exactly’ Patient code
No. of adjectives used for phantom limb pain
No. of adjectives used for stump pain
No. of adjectives used to describe both types of pain
JJ PF MB AR TK GG WK JP GL KH
11 13 9 6 5 8 6 11 16 5
7 5 9 21 7 8 11 3 – 3
7 5 5 5 4 3 1 1 0 0
(Table 3). Although, in general, both types of pain were described with similar terms, the number of common descriptors (fourth column of the table) compared to the total number of terms used to describe either phantom limb (second column) or stump pain (third column) is small. The most frequently used terms to describe both phantom limb and stump pain were burning, convulsive, hot, searing, throbbing and intense. Again, most of these descriptors refer to the sensory rather than to the affective quality of pain. 3.4. Relationship between stump pain and phantom limb pain. Twelve patients with phantom limb pain (75.0%) reported stump pain at the time of the interview, while only one patient without phantom limb pain (6.3%) reported stump pain at that time (Yates corrected x2 = 10.87, P , 0.01). This incidence rate was similar to that reported when amputees were retrospectively asked about stump pain after the amputation (11 with phantom limb pain and three without, respectively; Yates corrected x2 = 7.87, P , 0.01). Nine patients (81.8%) reported that stump pain lasted a few seconds to minutes; only two patients (18.2%) suffered longer periods of pain. Stump pain was experienced daily or continuously in four cases (36.4%), and from several times per week to more seldom in seven cases (63.6%). The mean intensity of phantom limb pain at the time of the interview for patients experiencing stump pain was 4.9 (on a 10-cm VAS scale, SD = 2.5, range: 1.1–8.8 cm) and for stump pain the intensity was 4.7 (SD = 2.5, range: 0.4–8.5 cm). Thus, for patients experiencing stump pain at the time of the interview, the intensity of phantom limb and stump pain was similar. A significant positive correlation was found between the intensity of phantom limb pain and stump pain experienced at the time of the interview (Pearson r = 0.77, P , 0.01). The mean pain intensities that were recalled for the time immediately after amputation were also similar: 6.2 for phantom limb pain (SD = 2.4, range:
(convulsive, hot, searing, wrenching, heavy, dreadful, intense) (burning, throbbing, beating, pounding, intense) (burning, convulsive, hot, stabbing, tingling) (burning, searing, beating, pounding, unbearable) (burning, hot, searing, dreadful) (convulsive, throbbing, gruelling) (throbbing) (intense)
2.1–9.7 cm) and 6.2 for stump pain (SD = 2.8, range: 0.5– 9.5 cm). Moreover, the intensity of pain recalled for the period shortly after amputation showed a positive correlation with the intensity of pain just before the interview (for phantom limb pain: Pearson r = 0.64, P , 0.05; for stump pain: Pearson r = 0.74, P , 0.05). Thus, high ratings of current pain were associated with high ratings of pain intensities recalled for the period shortly after amputation in phantom limb pain subjects. In addition, repeated measures ANOVAs with the within-subjects factor Time revealed that for both kinds of pain, the intensity of the pain recalled for the period after amputation was greater than the pain intensity experienced during the period just before the time of the interview (phantom limb pain: F(1,13) = 5.5, P , 0.05; stump pain: F(1,9) = 11.2, P , 0.01). 3.5. Other measures The mean scores obtained on three scales of the West Table 4 Mean and standard deviations for three MPI scales. Data are from 16 agematched chronic back pain patients randomly obtained from a sample of 239 subjects reported by Flor and Birbaumer, 1995. In amputees, ratings were obtained separately for phantom limb and stump pain
Pain Severity Phantom limb pain* Stump pain* Chronic back pain Interference Phantom limb pain* Stump pain* Chronic back pain Support Phantom limb pain Stump pain Chronic back pain
Mean
SD
1.7 1.3 3.1
1.2 0.9 0.8
1.2 1.1 2.7
1.1 1.3 1.3
3.0 3.0 3.6
1.9 2.2 1.5
*Indicates statistically significant differences (P , 0.01) between this amputee sample and the chronic pain sample (n = l6) of Flor and Birbaumer, 1995.
92
P. Montoya et al. / Pain 72 (1997) 87–93
Haven Yale Multidimensional Pain Inventory (MPI) for phantom limb and stump pain are shown in Table 4. These scores were compared with those of a subsample of 16 age-matched chronic low back pain patients from a previous study (Flor and Birbaumer, 1995). Significant group differences were found in the scales Pain Severity and Interference, indicating that amputees showed lower pain levels (for both phantom limb and stump pain) than chronic low back pain patients. No group differences were found in the scale Support. No statistically significant differences were found in the vividness of mental imagery between amputees with and without phantom limb pain for any of the categories of sensory experience measured. However, a positive correlation (Spearman r = 0.56, P , 0.05) was found in amputees with phantom limb pain between the intensity of phantom limb pain and the vividness ratings of movements with the phantom hand.
4. Discussion The results of the present study revealed a positive association between phantom limb pain and non-painful phantom limb sensations (such as cutaneous sensations, position, and movements). An increased intensity of phantom limb pain was associated with more intense non-painful phantom limb sensations. This is in accordance with the data showing that there are quantitative and qualitative differences in the descriptions of painful and non-painful phantom limb sensations (Katz and Melzack, 1991; Katz, 1992). In our sample, a similar number of amputees with and without phantom limb pain reported telescoping. Moreover, we observed four patients with very strong and continuous phantom limb pain who experienced a constant and intense perception of telescoping. These data are consistent with clinical data from Poeck (1963), who noted that 36 out of 40 patients who reported strong phantom limb pain also reported a shrinkage of the phantom limb. Our data do not support early observations (Riddoch, 1941; Henderson and Smyth, 1948) and the suggestion of Katz (1992) that phantom limb pain prevents or retards telescoping. Moreover, aspects of the data in these three studies are problematic. Thus, Henderson and Smyth’s (1948) report is based on the authors’ recollection of data obtained several years earlier during World War II in prisoner-of-war hospitals and camps in Germany. Riddoch (1941) wrote that telescoped phantom limbs often return to a normal position when phantom limb pain appears. Nevertheless, he also noted that sometimes a painful phantom limb ‘appear(s) to be nearer to the stump than it ought to be’ (p. 203). In a study of referred sensations elicited by electrical stimulation in chronic pain patients, Katz and Melzack (1987) observed a patient (case 57) who reported telescoping of his right lower arm and hand upon electrical stimulation of his right ear. The telescoping of the limb was maintained for at least 3 years, but no
information about pain changes was given. Katz (1992) later hypothesized that perceptual changes in the length and size of the phantom limb might be a correlate of the cortical reorganization that has been observed in animals (Merzenich et al., 1984). However, recent evidence (Flor et al., 1995; Knecht et al., 1995, 1996) indicates that the magnitude of these neuroplastic changes in the somatosensory cortex is not correlated with telescoping or non-painful referred sensations (though they are strongly correlated with the amount of phantom limb pain that is experienced). Phantom limb pain and stump pain differed in both intensity and quality. Amputees chose more sensory adjectives (stabbing, beating, searing, convulsive, throbbing, hot, burning) to describe their phantom limb pain than affective terms (intense, gruelling, heavy, annoying, etc.); however, no differences were found between these two pain dimensions for the description of stump pain. In addition, only a small proportion of common adjectives was considered appropriate for the description of both types of pain when they were experienced by the same individual. As shown in Table 2, the sensory qualities of phantom limb pain were also more varied than those of stump pain. Several sensory adjectives were used to describe phantom limb pain by more than 50% of phantom limb pain patients; whereas only the description of stump pain as ‘hot’ was chosen by more than 50% of subjects suffering from stump pain. These data provide support for the formulation by Melzack (1989) that phantom limbs, whether painful or painless, constitute an elaborate percept suggesting that it is generated by a complex perceptual neural network. Subjects were asked to retrospectively describe the quality and intensity of the pain experienced immediately after the amputation. No data on pain ratings made at that time are available; therefore, it is not possible to determine what the influence of memory distortion (Erskine et al., 1990) might be. It has been found that when pain is chronic, it may lead to an overestimation of past pain (Erskine et al., 1990; Bryant, 1993), though the fading of pain memories is also a well-known phenomenon. Thus, the finding that the intensity of the remembered pain was significantly higher here than the intensity of the pain being currently experienced could be due to memory distortion. However, other aspects of the data indicate that the subjects in this study made differential judgments of change over time with respect to different aspects of painful and non-painful phantom limb sensations. This suggests that the report of greater phantom limb pain at the time of the amputation than in the chronic situation (at the time of the interview) may well be veridical. The relationship between chronic phantom limb pain and other chronic pain syndromes has not yet been established. The results of the MPI scales indicate that amputees with chronic pain report less intense pain than chronic back pain patients. It is possible that phantom limb pain is less intense than chronic back pain. Another possible explanation is that patients with phantom limb pain typically experience an
P. Montoya et al. / Pain 72 (1997) 87–93
episodic occurrence of pain attacks as compared to back pain patients who often suffer from more continuous or more frequent pain; this may influence the judgment of intensity. Further results of the present study indicate that there is a significant positive relationship between the occurrence and intensity of stump pain and phantom limb pain. These findings are consistent with the observation of Sherman et al. (1984) that phantom limb pain occurs in conjunction with stump pain in approximately two-thirds of the amputees they studied, and that phantom limb pain is exacerbated by episodes of stump pain. As suggested by Sherman and Arena (1992), it is possible that peripheral factors influencing stump pain, such as blood flow and muscle tension changes, could be involved in many cases of phantom limb pain. This would not be incompatible with Melzack’s (1989) postulation of a neuromatrix or with data indicating that there is increased cortical excitability in phantom limb pain patients compared to pain-free amputees (Larbig et al., 1996), or with the finding that there is a very strong positive correlation between amount of cortical reorganization and magnitude of phantom pain (Flor et al., 1995; Knecht et al., 1996) and between peripheral input, cortical reorganization and phantom limb pain in a substantial proportion of amputees experiencing phantom limb pain. Both central and peripheral processes could interact to trigger and modulate painful and non-painful phantom limb sensations. The determination of the nature of this interaction as well as the causal contribution of each of these components is a significant question awaiting future research. Acknowledgements The authors would like to thank Prof. Peter Rosenfeld at Northwestern University in Evanston (USA) and two anonymous reviewers for their helpful comments, and Ms. Dietlinde Stahl for her assistance during data acquisition.
References Bryant, R.A., Memory for pain and affect in chronic pain patients, Pain, 54 (1993) 347–351. Carlen, P., Wall, P., Nadvorna, H. and Steinbach, T., Phantom limbs and related phenomena in recent traumatic amputations, Neurology, 28 (1978) 211–217. Erskine, A., Morley, S. and Pearce S., Memory for pain: review, Pain, 41 (1990) 255–266. Flor, H. and Birbaumer, N., Psychobiologie und interdisziplina¨re Therapie chronischer Wirbelsa¨ulensyndrome, GSF-Forschungszentrum fu¨r Umwelt und Gesundheit, GmbH, Mu¨nchen, 1995. Flor, H., Rudy, T.E., Birbaumer, N., Streit, B. and Schugens, M.M., Zur
93
Anwendbarkeit des West Haven-Yale Multidimensional Pain Inventory im deutschen Sprachraum, Der Schmerz, 4 (1990) 82–87. Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., Larbig, W. and Taub, E., Phantom limb pain as a perceptual correlate of cortical reorganization following arm amputation, Nature, 375 (1995) 482–484. Geissner, E., Die Schmerzempfindungsskala, PVU, 1997 (in press). Gue´niot, M., D’une hallucination du touche (ou he´te´rotopie subjective des extre´mite´s) particulie`re a certains ampute´s, Journal de la physiologie de l’homme et des animaux, 4 (1861) 416–430. Henderson, W.R. and Smyth, G.E., Phantom limbs, J. Neurol. Neurosurg. Psychiatry, 2 (1948) 88–112. Jensen, T. and Rasmussen, P., Phantom pain and related phenomena after amputation. In: P.D. Wall and R. Melzack (Eds.), Textbook of Pain, 3rd ed., Churchill Livingstone, New York, 1994, pp. 651–665. Jensen, T., Krebs, B., Nielsen, J. and Rasmussen, P., Immediate and longterm phantom limb pain in amputees: incidence, clinical characteristics and relationship to preamputation limb pain, Pain, 21 (1985) 267–278. Katz, J., Psychophysiological contributions to phantom limbs, Can. J. Psychiatry, 37 (1992) 282–298. Katz, J. and Melzack, R., Referred sensations in chronic pain patients, Pain, 28 (1987) 51–59. Katz, J. and Melzack, R., Auricular transcutaneous electrical nerve stimulation (TENS) reduces phantom limb pain, J. Pain Symptom Manage., 6 (1991) 73–83. Kerns, R.D., Turk, D.C. and Rudy, T.E., The West Haven Multidimensional Pain Inventory (WHYMPI), Pain, 23 (1985) 345–356. Knecht, S., Henningsen, H., Elbert, T., Flor, H., Ho¨hling, C., Pantev, C., Birbaumer, N. and Taub, E., Cortical reorganization in human amputees and mislocalization of painful stimuli to the phantom limb, Neurosci. Lett., 201 (1995) 262–264. Knecht, S., Henningsen, H., Elbert, T., Flor, H., Ho¨hling, C., Pantev, C. and Taub, E., Reorganization and perceptual changes after amputation, Brain, 119 (1996) 1213–1219. Larbig, W., Montoya, P., Flor, H., Bilow, H., Weller, S. and Birbaumer, N., Evidence for a change in neural processing in phantom limb pain patients, Pain, 67 (1996) 275–283. Melzack, R., The McGill Pain Questionnaire: major properties and scoring methods, Pain, 1 (1975) 277–299. Melzack, R., Phantom limbs, the self, and the brain (The D.O. Hebb memorial lecture), Can. Psychol., 30 (1989) 1–16. Merzenich, M.M., Nelson, R.J., Stryker, M.P., Cynader, M.S., Shoppmann, A. and Zook, J.M., Somatosensory cortical map changes following digit amputation in adult monkeys, J. Comp. Neurol., 224 (1984) 591–605. Poeck, K., Phantome nach Amputation und bei angeborenem Gliedmassenmangel, Dtsch. Med. Wochenschr., 94 (1963) 2367–2374. Riddoch, G., Phantom limbs and body shape, Brain, 64 (1941) 197– 222. Sheehan, P.W., A shortened form of Betts’ Questionnaire upon Mental Imagery, J. Clin. Psychol., 23 (1967) 386–389. Sherman, R.A. and Sherman, C.J., Prevalence and characteristics of chronic phantom limb pain among American veterans, Am. J. Phys. Med., 62 (1983) 227–238. Sherman, R.A., Sherman, C.J. and Parker, L., Chronic phantom and stump pain among American veterans: results of a survey, Pain, 18 (1984) 83– 95. Sherman, R.A. and Arena, J.G., Phantom limb pain: mechanisms, incidence and treatment, Crit. Rev. Physical Rehabil. Med., 4 (1992) 1– 26. Weiss, S.A. and Fishman, S., Extended and telescoped phantom limbs in unilateral amputees, J. Abn. Soc. Psychol., 66 (1963) 489–497.
The relationship of phantom limb pain to other phantom limb phenomena in upper extremity amputees1 Pedro Montoya a ,*, Wolfgang Larbig a, Norbert Grulke a, Herta Flor b, Edward Taub c, Niels Birbaumer a , d a
Institute of Medical Psychology and Behavioral Neurobiology, University of Tu¨bingen, Gartenstrasse 29, D-72074 Tu¨bingen, Germany b Department of Psychology, Humboldt University, Berlin, Germany c Department of Psychology, University of Alabama at Birmingham, Birmingham, USA d Department of General Psychology, University of Padova, Padova, Italy Received 1 February 1997; revised version received 24 February 1997; accepted 19 March 1997
Abstract In thirty-two unilateral upper extremity amputees with and without phantom limb pain, various phantom limb phenomena were investigated. In general, the incidence of non-painful phantom limb sensations was higher in patients with phantom limb pain than in pain-free amputees. Kinesthetic and kinetic phantom limb sensations were reported more frequently than exteroceptive cutaneous sensations. There was a significant positive correlation between phantom limb pain and stump pain. Patients more frequently assigned sensory than affective pain qualities to their phantom limb pain, whereas no differences between pain qualities were observed for stump pain. No support was found for a relationship between the presence of telescoping (i.e., shrinkage of the phantom limb) and phantom limb pain. These findings point to central as well as to peripheral factors contributing to phantom limb pain. 1997 International Association for the Study of Pain. Published by Elsevier Science B.V. Keywords: Upper extremity amputation; Phantom limb pain; Phantom limb sensation; Stump pain; Telescoping; Pain qualities
1. Introduction For many individuals, the most distressing problem after amputation is the continuing experience of phantom limb sensations, especially if these sensations are painful. According to several surveys (Carlen et al., 1978; Sherman and Sherman, 1983; Sherman et al., 1984; Jensen et al., 1985), phantom limb sensations are reported by 70–100% of amputees, and phantom limb pain occurs in 60–85% of these cases. Phantom limb sensations are commonly described as tingling, numbness, pins and needles, burning, cramping, squeezing, or itching. Changes in the length, size, temperature, volume, or position of the phantom limb are also frequently reported. About one-third of the amputee
* Corresponding author. Tel.: +49 7071 29 74226; fax: +49 7071 29 5956; email: [email protected] 1 This work was supported by the Deutsche Forschungsgemeinschaft (Research Group ‘Clinical Psychophysiology of Pain’, Bi 195/24).
population experiences a bizarre phenomenon called telescoping (Weiss and Fishman, 1963; Katz, 1992; Jensen and Rasmussen, 1994). This process refers to the gradual shrinking of the phantom limb so that distal parts of the phantom limb seem to approach the stump; later the phantom foot or hand may seem to retract or even disappear completely into the stump, but can still be perceived as a foot or hand (Gue´niot, 1861; Henderson and Smyth, 1948). It has been postulated that the experience of telescoping is inversely related to phantom limb pain, such that telescoping is reduced or absent when phantom limb pain is present (Riddoch, 1941; Henderson and Smyth, 1948; Weiss and Fishman, 1963; Katz and Melzack, 1987; Katz, 1992; Jensen and Rasmussen, 1994). Katz and Melzack (1987) reported a single case with severe phantom limb pain who experienced telescoping of the phantom limb during electrical stimulation of both ears which was paralleled by satisfactory pain relief. The goal of the present study was to investigate some of the characteristics of painful and non-painful phantom limb
0304-3959/97/$17.00 1997 International Association for the Study of Pain. Published by Elsevier Science B.V. PII S0304-3959 (97 )0 0004-3
88
P. Montoya et al. / Pain 72 (1997) 87–93
sensations, as well as the relationship of phantom limb pain with stump pain. We sought to evaluate the question of whether phantom limb pain and phantom limb sensations are closely related.
2. Methods 2.1. Subjects Sixty-five amputees who were registered as clients of an orthopedic appliance shop that fitted amputees with prostheses were contacted by telephone. A brief interview was used to select those subjects who met the following criteria: (a) unilateral upper-limb amputation, (b) between 18 and 60 years of age, (c) absence of any diagnosed psychiatric disorder, and (d) taking no current medication. Thirty-two unilateral upper-limb amputees (three female) with a mean age of 41.0 years (SD = 11.7, range: 20–58 years) participated in the study. With the exception of two cases of congenital limb deficiency, subjects had undergone amputation as a result of an accident. The time elapsed since the traumatic amputation ranged from 10 months to 49 years, with a mean of 12.2 years (SD = 10.5). The subjects were reimbursed for travel expenses and informed consent was obtained after the nature and purpose of the study were explained. 2.2. Measures 2.2.1. Assessment of phantom limb and stump phenomena Two instruments were used to assess painful and nonpainful sensations experienced by amputees. 2.2.1.1. Phantom-and-Stump Phenomena Interview. The standardized Phantom-and-Stump Phenomena Interview developed by the authors (Flor et al., 1995) consists of 122 items that assess the location, quality, intensity, duration and frequency of phantom- and stump-related phenomena at the time of the interview and soon after amputation. It includes separate sections for painful and non-painful phantom limb sensations and for painful and non-painful stump sensations; thus, stump and phantom limb sensations were assessed separately. Phantom limb and stump pain are examined by: (a) pain descriptors based on the McGill Pain Questionnaire (Melzack, 1975) and derived from the Pain Sensitivity Scale2 (Geissner, 1997) which are scored for both appropriateness (4-point 2
This scale is a multidimensional instrument to assess the sensory and affective dimensions of pain. It consists of 24 pain descriptors which were modified from the McGill Pain Questionnaire. Both subscales show satisfactory internal consistency (Cronbachs’ a for the sensory and affective dimensions, 0.81 and 0.92, respectively) and good stability (test-retest correlations over 4 weeks, 0.95 and 0.96, respectively). For the present study, three additional descriptors (convulsive, tingling, wrenching) were included.
scale: 0 = ‘does not apply’, 1 = ‘applies a little’, 2 = ‘quite appropriate’, 3 = ‘applies exactly’), and frequency of occurrence (9-point scale: 0 = ‘never’ to 8 = ‘always’); (b) a 10-cm visual analogue scale (VAS) that describes the average intensity of pain ranging from ‘no pain’ to ‘unbearable pain’; and (c) a stylized human figure drawing on which the locations of regions of stump and phantom limb in which pain is experienced are indicated. In addition, non-painful stump and phantom limb sensations are assessed in the interview using: (a) 13 descriptors of sensations including kinesthetic (e.g., ‘I feel the size of the phantom limb’), kinetic (e.g., ‘I feel voluntary movements of the phantom limb’), and exteroceptive (e.g., ‘I feel pressure on the phantom limb’) sensations; each des-criptor was scored for both intensity (4-point scale: 0 = ‘no sensation’ to 3 = ‘very strong sensation’) and fre-quency (9-point scale: 0 = ‘never’ to 8 = ‘always’); (b) a 10-cm VAS to describe the average intensity of non-painful phantom limb and stump sensations ranging from ‘no sensation’ to ‘very strong sensation’; (c) a stylized human figure drawing to record the body regions from which non-painful phantom limb sensations were elicited and the location of regions of stump and phantom limb in which non-painful phantom or stump sensations were experienced; and (d) open-ended questions about possible factors influencing phantom limb and stump sensations. Additional items elicited detailed information about the presence of telescoping, the amount of telescoping (measured by calculating the distance from the phantom fingertips to the stump and referred to the intact arm), and the intensity and frequency of telescoping. 2.2.1.2. The West Haven-Yale Multidimensional Pain Inventory. The scales Pain Severity, Interference, and Support of The West Haven-Yale Multidimensional Pain Inventory (MPI; Kerns et al., 1985; German version Flor et al., 1990) were completed separately for stump and phantom limb pain experienced during the last week. 2.2.2. Evaluation of mental imagery. Patients’ ability to imagine stimuli in a variety of sensory modalities was assessed using a modified and shortened version of Betts’ Questionnaire upon Mental Imagery (QMI; Sheehan, 1967). This instrument was employed to determine whether there is a relationship between the vividness of patients’ imagery ability and the likelihood that they might experience phantom limb sensations. The original instrument investigates imagery in seven sensory modalities: visual, auditory, cutaneous, kinetic, gustatory, olfactory and organic. Subjects are instructed to consider carefully the image elicited by each item and rate its vividness on a 7-point scale (0 = ‘no image present at all’ to 6 = ‘perfectly clear and vivid’). In the present study, only items from the cutaneous (e.g., the prick of a pin) and the kinetic modalities (e.g., running upstairs) were used. In
P. Montoya et al. / Pain 72 (1997) 87–93
addition, 12 items were included to assess patients’ ability to imagine the characteristics and sensations of other persons (e.g., body form, the way of walking) and their own phantom and intact limbs (e.g., limb form, movement of the limb).
3. Results 3.1. Phantom limb pain According to the Phantom-and-Stump Phenomena Interview, 16 patients suffered from phantom limb pain both in the past and during the interview, 15 had never experienced phantom limb pain and one patient had occasionally experienced phantom limb pain during a period of 2 weeks before he left the hospital 4 months after amputation. Fourteen patients with phantom limb pain reported experiencing it since the first week after amputation. An additional patient had experienced pain for the first time more than 30 years after the amputation had been carried out. One phantom limb pain patient was not able to remember the onset of his pain. Fifteen patients reported that their phantom limb pain lasted a few seconds to minutes at a time; only one patient suffered from longer periods of pain (several hours). Phantom limb pain was experienced every day at frequent intervals by five patients (31%), while eleven (69%) reported phantom limb pain from several times per day to approximately once per week. Table 1 presents demographic characteristics of the phantom limb pain and the pain-free group. There were no significant group differences in age, time since amputation, gender, site of the amputation (above versus below elbow), or educational level. Table 1 Demographic variables
Age (years) Mean SD Range Time since amputation (years) Mean SD Range Gender Female Male Amputation site Above elbow Below elbow Educational level (school) More than 8 years Less than 8 years
Amputees with phantom limb pain (n = 16)
Amputees without phantom limb pain (n = 16)
42.3 12.5 20–58
40.0 11.2 23–57
10.6 11.3 1–49
12.2 10.2 0–36
– 16
3 13
5 11
3 13
15 1
15 1
89
3.2. Non-painful phantom limb sensations Non-painful phantom limb sensations were reported at the time of the investigation by all 16 patients with phantom limb pain and 10 patients without phantom limb pain. The difference between groups was significant (Yates corrected x2 = 7.15, P , 0.01). A significant group difference was also found in retrospective reports of non-painful phantom limb sensations shortly after the amputation; 16 phantom limb pain and 8 pain-free subjects, respectively, indicated non-painful phantom limb sensations at that time (Yates corrected x2 = 10.33, P , 0.01). Six patients (including the two congenital amputees) reported never having either painful or non-painful phantom limb sensations. In order to investigate in more detail the nature of phantom limb sensations as well as changes from the time of the amputation to the time of the interview, we computed the product (ranging from 0 to 24) of the intensity and frequency for the three categories of phantom limb sensations (kinesthetic, kinetic, exteroceptive) from the Phantom-andStump Phenomena Interview. A three-way ANOVA was performed on this measure; the between-subjects factor was Group (phantom limb pain versus no phantom limb pain) and within-subjects factors were Category (kinesthetic, kinetic, exteroceptive) and Time (shortly after amputation versus at present). A significant Category effect was found (F(2,42) = 12.7, P , 0.001, Greenhouse-Geisser epsilon = 0.9): the mean kinesthetic phantom sensation was 8.5 on a scale ranging from 0 to 24 (SD = 6.7), the mean kinetic phantom sensation was 6.7 (SD = 5.5) and the mean exteroceptive phantom sensation was 1.9 (SD = 3.0). Post-hoc analyses indicated that the magnitude of exteroceptive phantom limb sensations was significantly lower than that of kinesthetic (t-test (25) = 5.1, P , 0.001) and kinetic (t-test (25) = 5.1, P , 0.001) sensations, but there was no difference between kinesthetic and kinetic sensations (t-test (25) = 1.5, NS). A marginally significant Group effect was found (F(1,21) = 3.9, P = 0.063) for the intensity of non-painful phantom sensations: amputees with phantom limb pain tended to report more intense non-painful phantom sensations (mean = 7.3, SD = 3.8) than painfree amputees (mean = 3.1, SD = 2.9). The reason for the marginal nature of this group effect was that there was a significant difference in the intensity of non-painful phantom limb sensations between patients with phantom limb pain and those without phantom limb pain at the time of the interview (F(l,23) = 7.4, P , 0.05); but this difference between groups was not significant immediately after amputation (F(1,22) = 2.8, P . 0.1). Moreover, a significant positive correlation was found between the intensity of phantom limb pain and the magnitude (product of intensity and frequency) of non-painful phantom limb sensations (Spearman r = 0.57, P , 0.05). This provides further evidence that increased phantom limb pain is associated with stronger non-painful phantom limb sensations. A significant Time effect (F(1,21) = 4.8, P , 0.05) was present when the
90
P. Montoya et al. / Pain 72 (1997) 87–93
frequency, but not the intensity of non-painful phantom limb sensations was examined separately: non-painful phantom limb sensations were more frequent immediately after amputation (mean = 3.8 on a scale ranging from 0 to 8, SD = 1.4) than at the time of the study (mean = 3.1, SD = 1.5); this was not the case for the intensity of nonpainful phantom limb sensations. Twelve patients (of 16) with phantom limb pain and five (of 10) pain-free amputees reported telescoping of the phantom limb (Yates corrected x2-square = 1.63, NS). When it occurred, the sensation of telescoping was quite intense, and there was no difference in experienced intensity for patients with phantom limb pain (mean = 8.6 cm on a 10-cm VAS, SD = 2.2) and pain-free amputees (mean = 7.9 cm, SD = 3.7). There was also no significant group difference with respect to the length of the telescoped phantom limb measured as the percentage of shrinkage from the phantom fingertips to the stump compared to the intact arm (a value of 100% indicates that the phantom limb is perceived within Table 2 Percentage of amputees who considered the different items of the Pain Sensitivity Scale (Geissner, 1997) to be ‘quite appropriate’ or ‘applies exactly’ to describe their phantom limb pain and stump pain Phantom limb pain recalled
Sensory dimension Stabbing Beating Searing Convulsive Throbbing Hot Burning Pounding Penetrating Tingling Wrenching Cutting Tearing Affective dimension Intense Gruelling Heavy Annoying Terrible Unbearable Dreadful Cruel Torturing Wretched Exhausting Horrible Petrified Killing
Stump pain recalled
After amputation
At the time of After the interview amputation
At the time of the interview
73.3 60.0 73.3 73.3 73.3 66.7 60.0 53.3 53.3 46.7 53.3 46.7 26.7
75.0 68.8 62.5 62.5 56.3 56.3 56.3 43.8 37.5 31.3 25.0 25.0 12.5
57.1 71.4 71.4 42.9 64.3 64.3 57.1 50.0 28.6 64.3 50.0 35.7 42.9
36.4 36.4 36.4 36.4 45.5 54.5 36.4 27.3 18.2 27.3 36.4 36.4 36.4
80.0 66.7 46.7 53.3 46.7 46.7 33.3 40.0 6.7 33.3 26.7 13.3 13.3 13.3
50.0 37.5 37.5 31.3 18.8 18.8 18.8 12.5 12.5 6.3 6.3 6.3 – –
71.4 57.1 50.0 57.1 64.3 28.6 64.3 35.7 42.9 35.7 35.7 42.9 7.1 14 3
45.5 27.3 18.2 – 36.4 5.9 45.5 18.2 18.2 18.2 18.2 27.3 11.8 –
the stump; a value of 0% refers to a non-telescoped limb and indicates that the phantom limb is perceived as having the same length as the intact arm). For patients with phantom limb pain who had telescoping, the mean shrinkage was 84.2% (SD = 21.1); for pain-free amputees who had telescoping, the mean shrinkage was 99.0% (SD = 2.2) (Yates corrected x2 = 1.23, NS). 3.3. Pain Quality Table 2 presents the percentage of patients who considered each of the different adjectives of the Pain Sensitivity Scale to be ‘quite appropriate’ (score of 2 on a 0–3 numerical scale) or "apply exactly’ (score of 3) to describe their phantom limb pain (left side of table) and stump pain (right side). As can be seen, more descriptors from the sensory subscale than from the affective subscale were chosen by at least 50% of the amputees as being appropriate. In addition, adjectives used to describe pain shortly after amputation were more varied than those used to describe current pain. The mean score of the appropriateness of pain descriptors was calculated for the sensory and the affective dimensions and a two-way ANOVA3 for repeated measures was carried out separately for phantom limb pain and stump pain on this measure, the factors being Pain Quality (sensory versus affective) and Time (at present versus soon after amputation). A significant Pain Quality effect was found (F(1,13) = 25.52, P , 0.001): sensory qualities were considered more appropriate to describe phantom limb pain (mean = 1.5 on a scale ranging from 0 to 3, SD = 0.6) than affective qualities (mean = 0.9, SD = 0.6). A significant Time effect was also found (F(1,13) = 6.96, P , 0.05), indicating that all pain descriptors were considered less appropriate at the time of the interview (mean = 1.0, SD = 0.4) than they were for the recall of the pain experience at the time of the amputation (mean = 1.4, SD = 0.6). The Pain Quality × Time effect did not achieve significance (F(1,13) = 3.2, P , 0.1). No significant differences were found in the appropriateness of sensory and affective descriptors for stump pain (Pain Quality effect: F(1,10) = 2.0, NS). Moreover, both sensory and affective aspects of stump pain were considered less appropriate at the time of the interview (mean sensory = 1.2, SD = 0.6; mean affective = 0.8, SD = 0.6) as compared to the period immediately after the amputation (mean sensory = 1.7, SD = 0.7; mean affective = 1.3, SD = 0.8) (Time effect: F(1,10) = 10.7, P , 0.01). To evaluate whether patients who experienced both phantom limb and stump pain used the same or different descriptors for the two types of pain, the number of terms that were used for each type of pain was computed for each patient 3 Only patients reporting pain at both time points were included in this ANOVA, resulting in 14 patients for the analysis of phantom limb pain and 11 for stump pain.
91
P. Montoya et al. / Pain 72 (1997) 87–93 Table 3
Description of pain in patients experiencing both phantom limb and stump pain. Number of adjectives used to describe pain from the Pain Sensitivity Scale (Geissner, 1997) that were considered by the patients as ‘quite appropriate’ or ‘applies exactly’ Patient code
No. of adjectives used for phantom limb pain
No. of adjectives used for stump pain
No. of adjectives used to describe both types of pain
JJ PF MB AR TK GG WK JP GL KH
11 13 9 6 5 8 6 11 16 5
7 5 9 21 7 8 11 3 – 3
7 5 5 5 4 3 1 1 0 0
(Table 3). Although, in general, both types of pain were described with similar terms, the number of common descriptors (fourth column of the table) compared to the total number of terms used to describe either phantom limb (second column) or stump pain (third column) is small. The most frequently used terms to describe both phantom limb and stump pain were burning, convulsive, hot, searing, throbbing and intense. Again, most of these descriptors refer to the sensory rather than to the affective quality of pain. 3.4. Relationship between stump pain and phantom limb pain. Twelve patients with phantom limb pain (75.0%) reported stump pain at the time of the interview, while only one patient without phantom limb pain (6.3%) reported stump pain at that time (Yates corrected x2 = 10.87, P , 0.01). This incidence rate was similar to that reported when amputees were retrospectively asked about stump pain after the amputation (11 with phantom limb pain and three without, respectively; Yates corrected x2 = 7.87, P , 0.01). Nine patients (81.8%) reported that stump pain lasted a few seconds to minutes; only two patients (18.2%) suffered longer periods of pain. Stump pain was experienced daily or continuously in four cases (36.4%), and from several times per week to more seldom in seven cases (63.6%). The mean intensity of phantom limb pain at the time of the interview for patients experiencing stump pain was 4.9 (on a 10-cm VAS scale, SD = 2.5, range: 1.1–8.8 cm) and for stump pain the intensity was 4.7 (SD = 2.5, range: 0.4–8.5 cm). Thus, for patients experiencing stump pain at the time of the interview, the intensity of phantom limb and stump pain was similar. A significant positive correlation was found between the intensity of phantom limb pain and stump pain experienced at the time of the interview (Pearson r = 0.77, P , 0.01). The mean pain intensities that were recalled for the time immediately after amputation were also similar: 6.2 for phantom limb pain (SD = 2.4, range:
(convulsive, hot, searing, wrenching, heavy, dreadful, intense) (burning, throbbing, beating, pounding, intense) (burning, convulsive, hot, stabbing, tingling) (burning, searing, beating, pounding, unbearable) (burning, hot, searing, dreadful) (convulsive, throbbing, gruelling) (throbbing) (intense)
2.1–9.7 cm) and 6.2 for stump pain (SD = 2.8, range: 0.5– 9.5 cm). Moreover, the intensity of pain recalled for the period shortly after amputation showed a positive correlation with the intensity of pain just before the interview (for phantom limb pain: Pearson r = 0.64, P , 0.05; for stump pain: Pearson r = 0.74, P , 0.05). Thus, high ratings of current pain were associated with high ratings of pain intensities recalled for the period shortly after amputation in phantom limb pain subjects. In addition, repeated measures ANOVAs with the within-subjects factor Time revealed that for both kinds of pain, the intensity of the pain recalled for the period after amputation was greater than the pain intensity experienced during the period just before the time of the interview (phantom limb pain: F(1,13) = 5.5, P , 0.05; stump pain: F(1,9) = 11.2, P , 0.01). 3.5. Other measures The mean scores obtained on three scales of the West Table 4 Mean and standard deviations for three MPI scales. Data are from 16 agematched chronic back pain patients randomly obtained from a sample of 239 subjects reported by Flor and Birbaumer, 1995. In amputees, ratings were obtained separately for phantom limb and stump pain
Pain Severity Phantom limb pain* Stump pain* Chronic back pain Interference Phantom limb pain* Stump pain* Chronic back pain Support Phantom limb pain Stump pain Chronic back pain
Mean
SD
1.7 1.3 3.1
1.2 0.9 0.8
1.2 1.1 2.7
1.1 1.3 1.3
3.0 3.0 3.6
1.9 2.2 1.5
*Indicates statistically significant differences (P , 0.01) between this amputee sample and the chronic pain sample (n = l6) of Flor and Birbaumer, 1995.
92
P. Montoya et al. / Pain 72 (1997) 87–93
Haven Yale Multidimensional Pain Inventory (MPI) for phantom limb and stump pain are shown in Table 4. These scores were compared with those of a subsample of 16 age-matched chronic low back pain patients from a previous study (Flor and Birbaumer, 1995). Significant group differences were found in the scales Pain Severity and Interference, indicating that amputees showed lower pain levels (for both phantom limb and stump pain) than chronic low back pain patients. No group differences were found in the scale Support. No statistically significant differences were found in the vividness of mental imagery between amputees with and without phantom limb pain for any of the categories of sensory experience measured. However, a positive correlation (Spearman r = 0.56, P , 0.05) was found in amputees with phantom limb pain between the intensity of phantom limb pain and the vividness ratings of movements with the phantom hand.
4. Discussion The results of the present study revealed a positive association between phantom limb pain and non-painful phantom limb sensations (such as cutaneous sensations, position, and movements). An increased intensity of phantom limb pain was associated with more intense non-painful phantom limb sensations. This is in accordance with the data showing that there are quantitative and qualitative differences in the descriptions of painful and non-painful phantom limb sensations (Katz and Melzack, 1991; Katz, 1992). In our sample, a similar number of amputees with and without phantom limb pain reported telescoping. Moreover, we observed four patients with very strong and continuous phantom limb pain who experienced a constant and intense perception of telescoping. These data are consistent with clinical data from Poeck (1963), who noted that 36 out of 40 patients who reported strong phantom limb pain also reported a shrinkage of the phantom limb. Our data do not support early observations (Riddoch, 1941; Henderson and Smyth, 1948) and the suggestion of Katz (1992) that phantom limb pain prevents or retards telescoping. Moreover, aspects of the data in these three studies are problematic. Thus, Henderson and Smyth’s (1948) report is based on the authors’ recollection of data obtained several years earlier during World War II in prisoner-of-war hospitals and camps in Germany. Riddoch (1941) wrote that telescoped phantom limbs often return to a normal position when phantom limb pain appears. Nevertheless, he also noted that sometimes a painful phantom limb ‘appear(s) to be nearer to the stump than it ought to be’ (p. 203). In a study of referred sensations elicited by electrical stimulation in chronic pain patients, Katz and Melzack (1987) observed a patient (case 57) who reported telescoping of his right lower arm and hand upon electrical stimulation of his right ear. The telescoping of the limb was maintained for at least 3 years, but no
information about pain changes was given. Katz (1992) later hypothesized that perceptual changes in the length and size of the phantom limb might be a correlate of the cortical reorganization that has been observed in animals (Merzenich et al., 1984). However, recent evidence (Flor et al., 1995; Knecht et al., 1995, 1996) indicates that the magnitude of these neuroplastic changes in the somatosensory cortex is not correlated with telescoping or non-painful referred sensations (though they are strongly correlated with the amount of phantom limb pain that is experienced). Phantom limb pain and stump pain differed in both intensity and quality. Amputees chose more sensory adjectives (stabbing, beating, searing, convulsive, throbbing, hot, burning) to describe their phantom limb pain than affective terms (intense, gruelling, heavy, annoying, etc.); however, no differences were found between these two pain dimensions for the description of stump pain. In addition, only a small proportion of common adjectives was considered appropriate for the description of both types of pain when they were experienced by the same individual. As shown in Table 2, the sensory qualities of phantom limb pain were also more varied than those of stump pain. Several sensory adjectives were used to describe phantom limb pain by more than 50% of phantom limb pain patients; whereas only the description of stump pain as ‘hot’ was chosen by more than 50% of subjects suffering from stump pain. These data provide support for the formulation by Melzack (1989) that phantom limbs, whether painful or painless, constitute an elaborate percept suggesting that it is generated by a complex perceptual neural network. Subjects were asked to retrospectively describe the quality and intensity of the pain experienced immediately after the amputation. No data on pain ratings made at that time are available; therefore, it is not possible to determine what the influence of memory distortion (Erskine et al., 1990) might be. It has been found that when pain is chronic, it may lead to an overestimation of past pain (Erskine et al., 1990; Bryant, 1993), though the fading of pain memories is also a well-known phenomenon. Thus, the finding that the intensity of the remembered pain was significantly higher here than the intensity of the pain being currently experienced could be due to memory distortion. However, other aspects of the data indicate that the subjects in this study made differential judgments of change over time with respect to different aspects of painful and non-painful phantom limb sensations. This suggests that the report of greater phantom limb pain at the time of the amputation than in the chronic situation (at the time of the interview) may well be veridical. The relationship between chronic phantom limb pain and other chronic pain syndromes has not yet been established. The results of the MPI scales indicate that amputees with chronic pain report less intense pain than chronic back pain patients. It is possible that phantom limb pain is less intense than chronic back pain. Another possible explanation is that patients with phantom limb pain typically experience an
P. Montoya et al. / Pain 72 (1997) 87–93
episodic occurrence of pain attacks as compared to back pain patients who often suffer from more continuous or more frequent pain; this may influence the judgment of intensity. Further results of the present study indicate that there is a significant positive relationship between the occurrence and intensity of stump pain and phantom limb pain. These findings are consistent with the observation of Sherman et al. (1984) that phantom limb pain occurs in conjunction with stump pain in approximately two-thirds of the amputees they studied, and that phantom limb pain is exacerbated by episodes of stump pain. As suggested by Sherman and Arena (1992), it is possible that peripheral factors influencing stump pain, such as blood flow and muscle tension changes, could be involved in many cases of phantom limb pain. This would not be incompatible with Melzack’s (1989) postulation of a neuromatrix or with data indicating that there is increased cortical excitability in phantom limb pain patients compared to pain-free amputees (Larbig et al., 1996), or with the finding that there is a very strong positive correlation between amount of cortical reorganization and magnitude of phantom pain (Flor et al., 1995; Knecht et al., 1996) and between peripheral input, cortical reorganization and phantom limb pain in a substantial proportion of amputees experiencing phantom limb pain. Both central and peripheral processes could interact to trigger and modulate painful and non-painful phantom limb sensations. The determination of the nature of this interaction as well as the causal contribution of each of these components is a significant question awaiting future research. Acknowledgements The authors would like to thank Prof. Peter Rosenfeld at Northwestern University in Evanston (USA) and two anonymous reviewers for their helpful comments, and Ms. Dietlinde Stahl for her assistance during data acquisition.
References Bryant, R.A., Memory for pain and affect in chronic pain patients, Pain, 54 (1993) 347–351. Carlen, P., Wall, P., Nadvorna, H. and Steinbach, T., Phantom limbs and related phenomena in recent traumatic amputations, Neurology, 28 (1978) 211–217. Erskine, A., Morley, S. and Pearce S., Memory for pain: review, Pain, 41 (1990) 255–266. Flor, H. and Birbaumer, N., Psychobiologie und interdisziplina¨re Therapie chronischer Wirbelsa¨ulensyndrome, GSF-Forschungszentrum fu¨r Umwelt und Gesundheit, GmbH, Mu¨nchen, 1995. Flor, H., Rudy, T.E., Birbaumer, N., Streit, B. and Schugens, M.M., Zur
93
Anwendbarkeit des West Haven-Yale Multidimensional Pain Inventory im deutschen Sprachraum, Der Schmerz, 4 (1990) 82–87. Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., Larbig, W. and Taub, E., Phantom limb pain as a perceptual correlate of cortical reorganization following arm amputation, Nature, 375 (1995) 482–484. Geissner, E., Die Schmerzempfindungsskala, PVU, 1997 (in press). Gue´niot, M., D’une hallucination du touche (ou he´te´rotopie subjective des extre´mite´s) particulie`re a certains ampute´s, Journal de la physiologie de l’homme et des animaux, 4 (1861) 416–430. Henderson, W.R. and Smyth, G.E., Phantom limbs, J. Neurol. Neurosurg. Psychiatry, 2 (1948) 88–112. Jensen, T. and Rasmussen, P., Phantom pain and related phenomena after amputation. In: P.D. Wall and R. Melzack (Eds.), Textbook of Pain, 3rd ed., Churchill Livingstone, New York, 1994, pp. 651–665. Jensen, T., Krebs, B., Nielsen, J. and Rasmussen, P., Immediate and longterm phantom limb pain in amputees: incidence, clinical characteristics and relationship to preamputation limb pain, Pain, 21 (1985) 267–278. Katz, J., Psychophysiological contributions to phantom limbs, Can. J. Psychiatry, 37 (1992) 282–298. Katz, J. and Melzack, R., Referred sensations in chronic pain patients, Pain, 28 (1987) 51–59. Katz, J. and Melzack, R., Auricular transcutaneous electrical nerve stimulation (TENS) reduces phantom limb pain, J. Pain Symptom Manage., 6 (1991) 73–83. Kerns, R.D., Turk, D.C. and Rudy, T.E., The West Haven Multidimensional Pain Inventory (WHYMPI), Pain, 23 (1985) 345–356. Knecht, S., Henningsen, H., Elbert, T., Flor, H., Ho¨hling, C., Pantev, C., Birbaumer, N. and Taub, E., Cortical reorganization in human amputees and mislocalization of painful stimuli to the phantom limb, Neurosci. Lett., 201 (1995) 262–264. Knecht, S., Henningsen, H., Elbert, T., Flor, H., Ho¨hling, C., Pantev, C. and Taub, E., Reorganization and perceptual changes after amputation, Brain, 119 (1996) 1213–1219. Larbig, W., Montoya, P., Flor, H., Bilow, H., Weller, S. and Birbaumer, N., Evidence for a change in neural processing in phantom limb pain patients, Pain, 67 (1996) 275–283. Melzack, R., The McGill Pain Questionnaire: major properties and scoring methods, Pain, 1 (1975) 277–299. Melzack, R., Phantom limbs, the self, and the brain (The D.O. Hebb memorial lecture), Can. Psychol., 30 (1989) 1–16. Merzenich, M.M., Nelson, R.J., Stryker, M.P., Cynader, M.S., Shoppmann, A. and Zook, J.M., Somatosensory cortical map changes following digit amputation in adult monkeys, J. Comp. Neurol., 224 (1984) 591–605. Poeck, K., Phantome nach Amputation und bei angeborenem Gliedmassenmangel, Dtsch. Med. Wochenschr., 94 (1963) 2367–2374. Riddoch, G., Phantom limbs and body shape, Brain, 64 (1941) 197– 222. Sheehan, P.W., A shortened form of Betts’ Questionnaire upon Mental Imagery, J. Clin. Psychol., 23 (1967) 386–389. Sherman, R.A. and Sherman, C.J., Prevalence and characteristics of chronic phantom limb pain among American veterans, Am. J. Phys. Med., 62 (1983) 227–238. Sherman, R.A., Sherman, C.J. and Parker, L., Chronic phantom and stump pain among American veterans: results of a survey, Pain, 18 (1984) 83– 95. Sherman, R.A. and Arena, J.G., Phantom limb pain: mechanisms, incidence and treatment, Crit. Rev. Physical Rehabil. Med., 4 (1992) 1– 26. Weiss, S.A. and Fishman, S., Extended and telescoped phantom limbs in unilateral amputees, J. Abn. Soc. Psychol., 66 (1963) 489–497.